1887

Abstract

Sequence heterogeneities of variable positions located at regions V1 and V6 of 56 cloned 16S rRNA genes were determined from six strains. These nucleotides were involved in secondary structure base-pairing of stem-loops. Compensatory and single mutations have occurred but secondary structure was conserved. Eight different sequences were found in the stem at region V1 indicating that in these sites mutation rates are higher than those of homogenization processes. Region V6 showed two different structures (V6-I and V6-II) although heterogeneities were determined in nine sites. Strains ECOR52 and ECOR56 only showed the V6-I sequence, ECOR35 showed V6-II, whereas clones from ECOR42 and ECOR49 showed both types of V6 structures. Results were confirmed by PCR using V6 sequence-specific probes. Stem V6-II was also found in 16S rRNA sequences deposited in the RDP (Ribosomal Database Project) belonging to distantly related taxa; ancestral sequence V6-II seems to be homogenized in all operons of the multigene family of strain ECOR35 producing effects of distortion in the molecular clock, similar to those that homoplasies could produce. V6 sequence-specific probes were applied to the 72 ECOR strains: half showed both V6-I and V6-II, and the rest had one or another. Only strain ECOR24 did not yield products in the PCR test and sequencing of 12 cloned 16S rRNA genes revealed a third form, V6-III, also found in the RDP. Concerted evolution by homogenization of the rRNA family may induce chronometric distortions responsible for a loss of ultrametricity in phylogenetic trees, particularly, of very closely related micro-organisms.

Loading

Article metrics loading...

/content/journal/ijsem/10.1099/00207713-49-2-601
1999-04-01
2024-04-19
Loading full text...

Full text loading...

/deliver/fulltext/ijsem/49/2/ijs-49-2-601.html?itemId=/content/journal/ijsem/10.1099/00207713-49-2-601&mimeType=html&fmt=ahah

References

  1. Anton A. I., Martínez-Murcia A. J., Rodríguez-Valera F. 1998; Sequence diversity in the 16S-23S intergenic spacer region (ISR) of the rRNA operons in representatives of the Escherichia coli ECOR Collection. J Mol Evol 47:62–72
    [Google Scholar]
  2. Ash C., Farrow J. A. E., Wallbanks S., Collins M. D. 1991; Phylogenetic heterogeneity of the genus Bacillus revealed by comparative analysis of small-subunit-ribosomal RNA sequences. Lett Appl Microbiol 13:202–206
    [Google Scholar]
  3. Bascuñana C. R., Mattsson J. G., Bölske G., Johansson K.-E. 1994; Characterization of the 16S rRNA genes from Mycoplasma sp. strain F38 and development of an identification system based on PCR. J Bacteriol 176:2577–2586
    [Google Scholar]
  4. Böttger E. C. 1989; Rapid determination of bacterial ribosomal RNA sequences by direct sequencing of enzymatically amplified DNA. FEMS Microbiol Lett 65:171–176
    [Google Scholar]
  5. Brosius J., Palmer M. L., Kennedy J. P., Noller H. F. 1978 Complete nucleotide sequence of a 16S ribosomal RNA gene from Escherichia coliProc Natl Acad SciUSA 75:4801–4805
    [Google Scholar]
  6. Cammarano P., Palm P., Creti R., Ceccarelli E., Sanangelantoni A. M., Tiboni O. 1992; Early evolutionary relationships among known life forms inferred from elongation factor EF-2/EF-G sequences : phylogenetic coherence and structure of the archaeal domain. J Mol Evol 34:396–405
    [Google Scholar]
  7. Cilia V., Lafay B., Christen R. 1996; Sequence heterogeneities among 16S ribosomal RNA sequences and their effect on phylogenetic analyses at the species level. Mol Biol Evol 13:451–461
    [Google Scholar]
  8. Clayton R. A., Sutton G., Hinkle P. S. Jr, Bult C., Fields C. 1995; Intraspecific variation in small-subunit rRNA sequences in GenBank : shy single sequences may not adequately represent prokaryotic taxa. Int J Syst Bacteriol 45:595–599
    [Google Scholar]
  9. Desjardins P., Picard B., Kaltenböck B., Elion J., Denamur E. 1995; Sex in Escherichia coli does not disrupt the clonal structure of the population : evidence from random amplified polymorphic DNA and restriction-fragment-length polymorphism. J Mol Evol 41:440–448
    [Google Scholar]
  10. Dover G. 1982; Molecular drive: a cohesive mode of species evolution. Nature 299:111–117
    [Google Scholar]
  11. Dover G. 1987; DNA turnover and the molecular clock. J Mol Evol 26:47–58
    [Google Scholar]
  12. Dryden S. C., Kaplan S. 1990; Localization and structural analysis of the ribosomal RNA operons of Rhodobacter sphaeroides. Nucleic Acids Res 18:7267–7277
    [Google Scholar]
  13. Fleischmann R. D., Adams M. D., White O. 37 other authors 1995; Whole-genome random sequencing and assembly of Haemophilus influenzae Rd. Science 269:496–512
    [Google Scholar]
  14. Fox G. E., Wisotzkey J. D., Jurtshuk P. J. 1992; How close is close: 16S rRNA sequence identity may not be sufficient to guarantee species identity. Int J Syst Bacteriol 42:166–170
    [Google Scholar]
  15. García-Martfnez J., Martínez-Murcia A. J., Antón A. I., Rodríguez-Valera F. 1996; Comparison of the small 16S to 23S intergenic spacer region (ISR) of the rRNA operons of some Escherichia coli strains of the ECOR collection and E coli K-12. J Bacteriol 178:6274–6377
    [Google Scholar]
  16. Gogarten J. P., Kibak H., Dittrich P. 10 other authors 1989; Evolution of the vacuolar H+-ATPase: implications for the origin of eukaryotes. Proc Natl Acad SciUSA 86:6661–6665
    [Google Scholar]
  17. Gürtler V. 1993; Typing of Clostridium difficile strains by PCR-amplification of variable length 16S-23S rDNA spacer regions. J Gen Microbiol 139:3089–3097
    [Google Scholar]
  18. Gürtler V., Wilson V. A., Mayall B. C. 1991; Classification of medically important clostridia using restriction endonuclease site differences of PC-amplified 16S rDNA. J Gen Microbiol 137:2673–2679
    [Google Scholar]
  19. Gutell R. R., Larsen N., Woese C. R. 1994; Lessons from an evolving rRNA: 16S and 23S rRNA structures from a comparative perspective. Microbiol Rev 58:10–26
    [Google Scholar]
  20. Herzer P. J., Inouye S., Inouye M., Whittam T. S. 1990; Phylogenetic distribution of branded RNA-linked multicopy single-stranded DNA among natural isolates of Escherichia coli. J Bacteriol 172:6175–6181
    [Google Scholar]
  21. Hill C. W., Harnish B. W. 1981 Inversion between ribosomal RNA genes of Escherichia coliProc Natl Acad SciUSA 78:7069–7072
    [Google Scholar]
  22. Huysmans E., De Wachter R. 1986; Compilation of small ribosomal subunit RNA sequences. Nucleic Acids Res 14:73
    [Google Scholar]
  23. Iwabe N., Kuma K., Hasegawa M., Osawa S., Miuata T. 1989 Evolutionary relationship of archaebacteria, eubacteria and eukaryotes inferred from phylogenetic trees of duplicated genesProc Natl Acad SciUSA 86:9355–9359
    [Google Scholar]
  24. Kimura M. 1983 The Neutral Theory of Molecular Evolution Cambridge: Cambridge University Press;
    [Google Scholar]
  25. Kostman J. R., Edlind T. D., Lipuma J. J., Stull T. L. 1992; Molecular epidemiology of Pseudomonas cepacia determined by polymerase chain reaction ribotyping. J Clin Microbiol 30:2084–2087
    [Google Scholar]
  26. Lane D. J., Pace B., Olsen G. J., Stahl D. A., Sogin M. L., Pace N. R. 1985 Rapid determination of 16S ribosomal RNA sequences for phylogenetic analysisProc Natl Acad SciUSA 82:6955–6959
    [Google Scholar]
  27. Liefting L. W., Andersen M. T., Beever R. E., Gardner R. C., Forster R. L S. 1996; Sequence heterogeneity in the two 16S rRNA genes of Phormium yellow leaf phytoplasma. Appl Environ Microbiol 62:3133–3139
    [Google Scholar]
  28. Long E. O., David I. B. 1980; Repeated genes in eukaryotes. Annu Rev Biochem 49:727–764
    [Google Scholar]
  29. Maidak B. L., Larsen N., McCaughey M. J., Overbeek R., Olsen G. J., Foge K., Blandy J., Woese C. R. 1994; The ribosomal database project. Nucleic Acids Res 22:3485–3487
    [Google Scholar]
  30. Martínez-Murcia A. J. 1993; Phylogenetic analysis of the genera Leuconostoc and Aeromonas. PhD thesis, University of Reading
    [Google Scholar]
  31. Martínez-Murcia A. J., Benlloch S., Collins M. D. 1992; Phylogenetic interrelationships of members of the genera Aeromonas and Plesiomonas as determined by 16S ribosomal DNA sequencing: lack of congruence with results of DNADNA hybridizations. Int J Syst Bacteriol 42:412–421
    [Google Scholar]
  32. Murray R. G. E., Brenner D. J., Colwell R. R., De Vos P., Goodfellow M., Grimont P. A. D., Pfennig N., Stackebrandt E., Zavarzin G. A. 1990; International Committee on Systematic Bacteriology. Report of the ad hoc committee on approaches to taxonomy within the Proteobacteria. Int J Syst Bacteriol 40:213–215
    [Google Scholar]
  33. Mylvaganam S., Dennis P. P. 1992; Sequence heterogeneity between the two genes encoding 16S rRNA from the halophilic archaeobacterium Haloarcula marismortui. Genetics 130:399–410
    [Google Scholar]
  34. Ninet B., Monod M., Emler S., Pawlowski J., Metral C., Rohner P., Auckenthaler R., Hirschel B. 1996; Two different 16S rRNA genes in a mycobacterial strain. J Clin Microbiol 34:2531–2536
    [Google Scholar]
  35. Nübel U., Engelen B., Felske A., Snaidr J., Wieshuber A., Amann R. I., Ludwig W., Backhaus H. 1996; Sequence heterogeneities of genes encoding 16S rRNAs in Paenibacillus polymyxa detected by temperature gradient gel electrophoresis. J Bacteriol 178:5636–5643
    [Google Scholar]
  36. Ochman H., Selander R. K. 1984; Standard reference strains of Escherichia coli from natural populations. J Bacteriol 157:690–693
    [Google Scholar]
  37. Ohta T. 1991; Multi gene families and the evolution of complexity. J Mol Evol 33:34–41
    [Google Scholar]
  38. Olsen G. J., Woese C. R. 1993; Ribosomal RNA: a key to phylogeny. FASEB J 7:113–123
    [Google Scholar]
  39. Olsen G. J., Woese C. R., Overbook R. 1994; The winds of (evolutionary) change : breathing new life into microbiology. J Bacteriol 176:1–6
    [Google Scholar]
  40. Pettersson B., Johansson K.-E., Uhlén M. 1994; Sequence analysis of 16S rRNA from mycoplasmas by direct solid-phase sequencing. Appl Environ Microbiol 60:2456–2461
    [Google Scholar]
  41. Pettersson B., Leitner T., Ronaghi M., Bölske G., Uhlén M., Johansson K.-E. 1996; Phylogeny of the Mycoplasma mycoides cluster as determined by sequence analysis of the 16S rRNA genes from the two rRNA operons. J Bacteriol 178:4131–4142
    [Google Scholar]
  42. Pettersson B., Bölske G., Thiaucourt F., Uhlén M., Johansson K.-E. 1998; Molecular evolution of Mycoplasma capricolum subsp. capripneumoniae strains, based on polymorphisms in the 16S rRNA genes. J Bacteriol 180:2350–2358
    [Google Scholar]
  43. Picard B., Journet-Mancy C., Picard-Pasquier N., Goullet P. 1993; Genetic structures of the B2 and B1 Escherichia coli strains responsible for extra-intestinal infections. J Gen Microbiol 139:3079–3088
    [Google Scholar]
  44. Pühler G., Leffers H., Gropp F., Palm P., Klenk H.-P., Lottspeich F., Garrett R. A., Zillig W. 1989 Archaebacterial DNA-dependent RNA polymerases testify to the evolution of the eukaryotic nuclear genomeProc Natl Acad SciUSA 86:4569–4573
    [Google Scholar]
  45. Rössler D., Lugwig W., Schleifer K. H., Lin C., McGill T. J., Wisotzkey J. D., Jurtshuk J. R., Fox G. E. 1991; Phylogenetic diversity in the genus Bacillus as seen by 16S rRNA sequencing studies. Syst Appl Microbiol 14:266–269
    [Google Scholar]
  46. Ruimy R., Breittmayer V., Elbaze P., Lafay B., Boussemart O., Christen R. 1994; Phylogenetic analysis and assessment of the genera Vibrio Photobacterium Aeromonas and Plesiomonas deduced from small-subunit rRNA sequences. Int J Syst Bacteriol 44:416–426
    [Google Scholar]
  47. Sambrook J., Fritsch E. F., Maniatis T. 1989 Molecular Cloning: a Laboratory Manual, 2nd. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory;
    [Google Scholar]
  48. Sanger F., Nicklen S., Coulson A. R. 1977 DNA sequencing with chain-terminating inhibitorsProc Natl Acad SciUSA 74:5463–5467
    [Google Scholar]
  49. Sneath P. H. A. 1993; Evidence from Aeromonas for genetic crossing-over in ribosomal sequences. Int J Syst Bacteriol 43:626–629
    [Google Scholar]
  50. Stern S., Weiser B., Noller H. F. 1988; Model for the threedimensional folding of 16S ribosomal RNA. J Mol Bio I 204:447–481
    [Google Scholar]
  51. Stewart C. B. 1993; The powers and pitfalls of parsimony. Nature 361:603–607
    [Google Scholar]
  52. Suzuki Y., Yamada T. 1988; Study on rRNA genes in Mycobacterium smegmatis. Microbiol Immunol 32:1259–1262
    [Google Scholar]
  53. Syvanen M. 1987; Molecular clocks and evolutionary relationships : possible distortions due to horizontal gene flow. J Mol Evol 26:16–23
    [Google Scholar]
  54. Woese C. R. 1987; Bacterial evolution. Microbiol Rev 51:221–271
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/ijsem/10.1099/00207713-49-2-601
Loading
/content/journal/ijsem/10.1099/00207713-49-2-601
Loading

Data & Media loading...

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error